Morphology and quality of cultivated Laminaria japonica Aresch. in the temperate waters of Naruto Straits, Japan

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1 徳島水研報第 7 号 Bull. Tokushima. Pref. Fish. Res. Ins. No. 7, - 10 (2011) Morphology and quality of cultivated Laminaria japonica Aresch. in the temperate waters of Naruto Straits, Japan Masao OHNO *1, Akinori DAN *2, Ryoko YOSHIMOTO *3, Masayoshi MATSUOKA *4 Abstract Laminaria japonica constitutes one of the main species of edible seaweeds in Japan. Due to its increasing demand for high quality konbu, expansion of its cultivation grounds has been carried out successfully by transplantation from its natural beds in northern Japan (Hokkaido, Aomori) to the warm waters of southern Japan (Naruto Straits, Tokushima Prefecture). The present study compared the morphological characteristics and nutritive contents of the cultivated Laminaria in warm waters with those from the cold waters in Japan. Results showed that frond size (length, weight, width, thickness) and contents of protein, carbohydrates, lipids, and ash have comparatively similar values between cultivated and natural harvests. Forced-cultivation of Laminaria should therefore be able to meet the increasing demand for the seaweed in the future. Not only the two areas are comparable in size and qualities of their harvests, force-cultivation reduces the waiting time for harvesting. Key words: force-cultivation, Japan, konbu, Laminaria japonica, seaweed cultivation Introduction There are 18 species of Laminaria in Japan (Kawashima, 1984). The most valuable species, Laminaria japonica, occurs naturally in the cold waters of Japan. About 7 % (10,000 tons) of Laminaria are being harvested from the natural population while about 2 % comes from cultivation cold waters from cold to warm waters in Japan. It has been known that there are regional variations of the shape L. japonica fronds from different locations. Harima Sea Harima Konaruto Tokushima Pref. Kii Chan. 34º 34º Fukumura Awaji Is. 13º Wakayama Pref. The first transplanting experiment on L. japonica outside of its natural habitat in cold waters was in 1966 in the Seto Inland Sea, off Hyogo Prefecture, West Osaka (Ii et al., 1966). After then, Japanese fisheries researchers have carried out experimental cultivation of Laminaria in the warm waters. Much recently, the commercial cultivation of Laminaria is now being carried out in many warm water areas, but, so far, there are no reports of quality of harvests from these areas. In this paper, the morphology and qualities of cultivated Laminaria blades are compared among materials harvested from the new cultivation grounds in Naruto Strait and other fields Material and Methods The seedlings of Laminaria, produced in the indoor cul km Pacific Ocean Fig. 1 The location of the study site in the cost of Tokushima Prefecture. Closed circles indicate three cultivation areas. ture tanks of Iwate Seeding Center in northern Japan, were transferred to Naruto in November 2002, by air lift. The seeding strings were then cut into -cm segments, and inserted into the mother ropes at 0-cm interval. The mother ropes were then transplanted in the three cultivation fields in Naruto Strait, namely: Harima, Konaruto and Fukumura (Fig.1). Ten individuals having long frond lengths, which *1 Usa Marine Biological Institute, Kochi University, Usa-cho, Tosa, Kochi , Japan *2 Fisheries Research Institute, Tokushima Agriculture, Forestry and Fisheries Technology Center, Seto-cho, Naruto, Tokushima , Japan *3 Food Technology Division, Tokushima Prefectural Industrial Technology Center, 11-2, Nishibari, Saika-cho, Tokushima , Japan *4 Kaiyo Doboku Co., Ltd Tokushima Branch, Nakano-cho-4, Tokushima, Tokushima , Japan 13º N

2 Ohno et al. A B C Fig. 2 The frond cultivated in the cost of Tokushima Prefecture. A, Harima; B, Konaruto; C, Fukumura. Table 1 Average (± SD) length and weight of blade and stipe vis a vis the percentage maturation rate of cultivated Laminaria japonica in Tokushima Prefecture at three cultivations sites (n = 10) 1 m Cultivation area Harima Konaruto Fukumura Maturation rate (%) Blade length (cm) ±SD 23.3 ± ± ±9.2 Blade weight (g) ±SD 26.4 ± ± ±267.7 Stipe length (cm) ±SD. ± ± ±1.9 Stipe weight (g) ±SD 1.6 ± ± ±1. were selected from materials on June 2004 harvesting season, were used for the morphological analysis. Blade and stipe length, weight, width and thickness were measured in each material to find any possible morphological variants that may develop as a result of transplantation from cold to warm areas. The blade width and thickness were measured at 0-cm interval from 10 to 00-cm portion, i.e. from the base to the frond tip. Representative Laminaria fronds from the cultivation sites of Harima, Konaruto and Fukumura showing differences in morphology based on the above parameters were photodocumented. Determination of physico-chemical factors that affect algal growth was made in the cultivation areas from November 2003 to May 2004: Water temperature was recorded automatically using a self-registering thermometer (MDS- T, ALEC Electronics Co. Ltd.) at the Fisheries Research Institute near the Konaruto cultivation site. For salinity and nutrient analysis water samples were collected from the surface at each site and measured in the laboratory with a salinometer (MODEL3-G, Turumi Seiki Co. Ltd.) and an autoanalyzer (TRAACS800, Bran Rube Co. Ltd.), respectively. Moisture content of the fronds was determined as weight loss after drying the fronds to constant weight at 10 in an oven. Total nitrogen content was determined by the Kjeldahl method while crude protein was derived from the total nitrogen content multiplied by a factor of 6.2. Lipid content of the dried fronds (at 100 ) was extracted with a chloroform and methanol mixture (1:2) according to Southgate's method (Southgate, 1971). Ash content was estimated by heating the samples for hrs in a temperature-controlled muffle furnace at 0. The sum of the percentages of protein, moisture, fat (lipid) and ash was then subtracted from 100 g to obtain the percentage of carbohydrate in the sample. Results and discussion Cultivated Laminaria frond morphology Laminaria is characterized by its blade length, thickness and weight. The average blade length of the cultivated plants was lowest in Harima (23.3 cm), higher in Konaruto (377.3 cm) and highest in Fukumura (41.6 cm; Table 1). The average blade weight, likewise, was lowest in Harima (26.4 g), higher in Konaruto (703.1 g) and highest in Fukumura (92.8 g). The general appearance of the Lami- 6

3 Morphology and quality of cultivated Laminaria japonica in the temperate waters of Naruto Straits 3. Blade thickness ( mm ) Portion of blade ( cm ) Fig. 3 The changes in blade thickness from root to tip of Laminaria japonica., Harima;, Konaruto;, Fukumura Blade width ( cm ) Portion of blade ( cm ) Fig. 4 The changes in blade width from root to tip of Laminaria japonica., Harima;, Konaruto;, Fukumura. naria fronds from the three cultivation sites in Naruto, Tokushima Prefecture is shown in Fig. 2. In terms of stipe measurements, stipe length had lowest value in Harima (. cm), but unlike the blade length, highest value of stipe length was recorded in Konaruto (8. cm) instead of Fukumura (7.4 cm). Stipe weight, on the other hand, showed values from lowest to highest in Harima (1.6 g), Konaruto (3.8 g) and Fukumura (4.7 g; Table 1). The change in width from holdfast to the tip of L. japonica frond varied among the three study areas, but the width at the center of the blade showed almost similar values among the three areas (Fig. 3). Laminaria blades were at its thickest near the stipe-blade junction. Among the three cultivation areas in Naruto, those cultivated in Fukumura showed the highest values (2.7 mm) while those from Harima showed the lowest (1. mm) and those in Konaruto were of moderate thickness regardless of which portion of the blade the measurements were made, except for the 400-cm portion of the blade where the materials in Harima consisted of thicker blades than those in Konaruto (Fig. 4). Environmental conditions in the cultivation ground The seasonal changes of water temperature in Naruto Strait from November 2003 to May 2004 showed values lower than 10 in February (winter season) but this increased gradually towards the spring-summer season (reaching to about 20 in May) - the growing period of Laminaria in southern Japan. Harvest season of Laminaria blades is normally done in early June (Fig. ). Dissolved inorganic nitrogen (DIN) in the surface water of Laminaria cultivation areas showed higher values from November to December, ranging from 4.0μg-at L -1 to 6. μg-at L -1 in the three cultivation areas (Fig. 6). After this period, the DIN content decreased gradually during the growing season. The DIN contents in Harima showed highest concentration in the early growing season among the three cultivation areas. 7

4 Ohno et al. Water temperature ( ) Laminaria cultivation in each area was done off shore where the water current is very fast, brought about by the narrow Naruto Strait along the Seto Inland Sea. The cultivation area in Fukumura, has relatively faster water current observed among the three cultivation areas. The transplanted Laminaria were growing healthily at each commercial cultivation ground where in blade length increased with the increase in water temperature towards the spring season. The relative percentage (%) appearance of mature Laminaria harvested at the three cultivation areas is shown in Table 1. All of the blades harvested in Harima, did not mature as expected based on the absence of sori. Harvested blades showed maturation of 10 % and 30 % at Konaruto and Fukumura, respectively. As normally practiced, Laminaria fronds are harvested commercially before it reaches mature stage to avoid attachment of benthic animals. Nov. Dec. Jan. Feb. Mar. Apr Chemical composition May Fig. Changes of water temperature in Konaruto area. DIN (µg-at/l) Nov. Dec. Jan. Feb. Mar Fig. 6 Dissolved inorganic nitrogen (DIN) in the surface water near the cultivation grounds., Harima;, Konaruto;, Fukumura. The Laminaria fronds collected from the three study sites differed in terms of the amounts of general nutritive composition, namely: protein, lipid, carbohydrate and ash of Table 2 General nutritive composition of L. japonica cultivated in three sites along Naruto Strait, Tokushima Prefecture. Values are based on proximate analysis of 100 g dry weight sample weight sample Cultivation area Harima Konaruto Fukumura Water (%) Protein (%) Lipid (%) Carbohydrate (%) Ash (%) dry weight (Table 2). Relative amount, expressed as percentage (%), of water content did not show great difference among materials collected from the three sites. The materials from Fukumura, however, contained highest protein value (8.7 %) than those from Harima (.2%) and Konaruto (6.7%). Lipid content also did not vary much among materials collected from the three sites, which ranged from %. Carbohydrate contents, on the other hand, showed an opposite observation by comparison with protein content among the three sources. The content of carbohydrate in materials coming from Harima showed the highest value of 61.2% while those from Konaruto and Fukumura showed lower values of 4.3% and 49.1 %, respectively. The ash content of the analyzed materials had narrow range of %. Transplanting of Laminaria from its cold water origin of northern Japan to the warm water of southern Japan did not result to variation in thalli morphologies from those of its mother strain in the seed-farming center in Iwate. Thus, the results indicate that these characters, as stipe and blade length, weight, width and thickness in L. japonica are stable and are unchangeable by transplanting. Although blades of Laminaria harvested from Fukumura had fronds longer than those from Konaruto and Harima, despite the fact that nutrient contents in the cultivation areas were not so different, the longer fronds in Fukumura could be more of a result from the influence of stronger water current, promoting faster nutrient uptake in this area than with the other two areas in Naruto. The bigger blades grown in Naruto Strait might also be the effect of water temperature (8-20 ) during longer growing period from January to June. Comparison of morphological characteristics between the natural population of Laminaria in the cold waters of Hokkaido and Aomori and the fronds of cultivated Laminaria in Naruto (this survey) is shown in Table 3. The natural fronds of Laminaria in the fisheries grounds of Hokkaido and Aomori are normally harvested after two years (Sanbonsuga, 1984; Kirihara et al.,1989). The cultivated fronds in Naruto, in contrast, are harvested 7-8 8

5 Morphology and quality of cultivated Laminaria japonica in the temperate waters of Naruto Straits Table 3 Comparison of morphological characteristics among natural and cultivated Laminaria fronds in three areas of Japan Origin months after transplanting. These cultivated materials are called the forced-cultivated Laminaria. The frond size of the cultivated Laminaria in Fukumura is similar to those naturally grown in Hokkaido and Aomori; the width of the blades of the Naruto fronds was similar to the width of natural Laminaria blades in Hokkaido (Kawasima, 1984; Sanbonsuga, 1984). Blade length (cm) Blade width (cm) Blade fresh weight (g) * Hokkaido (natural) **Aomori (natural) Naruto (cultivated) *Sanbonsuga (1984), ** Kirihara et al. (1989) The most important quality of Laminaria products is their thickness. The natural fronds from Hokkaido has blade less than one mm thick in one year time and that range increases to between 3 and 4 mm in two years time (Kawasima, 1984). The blade thickness of cultivated fronds from Naruto (2.7 mm in Fukumura, 2.0 mm in Konaruto, and 1.7 mm in Harima) were relatively thin compared to those of the natural fronds growing in Hokkaido. But recently, their way of utilization differs between the 'northern' and the 'southern' types. The 'southern' (cultivated) Laminaria growing in Naruto Strait has soft texture compared to the 'northern' (natural) type growing in the cold waters. The latter is a preferred material over the former for preparing "oden" - a popular Japanese dish. The cultivation areas for Laminaria in warm waters in Japan have expanded quite recently where natural Laminaria population is absent. It is now possible to transfer by air lift the seeding string of Laminaria from the cold water seeding center in northern Japan to the warm water cultivation areas in southern Japan within 1-2 days. The data of blade length and water temperatures during cultivation period in several Laminaria cultivation areas in Japan are shown in Table 4. The size of cultivated blades is fairly different among cultivation areas. From these results, it can be concluded that the optimum water temperature of growing Laminaria could range from In addition, Kawashima (1984) reported that the optimum water temperature of naturally growing Laminaria in the cold waters of Hokkaiddo ranges from to 20. It is interesting to note that the forced Laminaria cultivation is recently being tried in the subtropical waters of Okinawa, Japan, as the water temperature in subtropical waters could also range from 16-2 for half a year. From these results, Laminaria cultivation can therefore Table 4 Comparison of blade length of Laminaria fronds in relation to temperature among the cultivation grounds during cultivation season Cultivation area Blade of length Lower water temperature High water temperature Sado Sakai (1968) Reference Yokosuka Torkko et al. (1987) Hyogo Ii et al. (1966) Naruto Matsuoka et al. (1991) Tosa Ohno & Matsuoka (1992) Ariake Yotusi & Nishikawa (1968) Ise Achiha & Nakamura (1988) Table General nutritive composition (per 100 dry wt.) of L. japonica from natural beds in Hokkaido Harvesting area Osatube (Hokkaido) Nisitoi (Hokkaido) Ohma (Aomori) Seawater (%) Protein (%) Lipid (%) Carbohydrate (%) Ash (%)

6 Ohno et al. be carried out in all coastal areas of Japan, i.e. from cold waters to warm waters. The quality of harvests based on frond characteristics, especially thickness, texture and taste could be used as basis in preparing different Japanese dishes. The natural L. japonica harvested in Hokkaido is considered of highest quality as it contain high protein and amino acids. From such commercial point of the view, it is therefore important to know if the forced cultivated Laminaria include protein content comparable to that of natural blades. The nutritive composition of dried Laminaria blades cultivated from different areas in Japan shows the different values among three sites. The larger blades cultivated in Fukumura shows the highest values of proteins and the best qualities among the three sites. Based on the relative percentage nutritive composition of the natural Laminaria fronds shown in Table the Naruto Laminaria fronds are therefore good harvesting grounds comparable in quality with those of natural harvests. The relative percentages of protein and carbohydrate among cultivated blades show similar values with those of the natural Laminaria (Sanbonsuga, 1984). Although the lipid content of the Naruto Laminaria fronds was lower than those of natural Laminaria its ash content from the same material was higher than that of natural fronds (Sanbonsuga, 1984). In conclusion, the results of size and nutritive contents of Laminaria show comparable results of forced-cultivated fronds with those from the natural grounds in the cold waters of Japan. Therefore force cultivation should be expanded to be able to meet the increasing demand for high quality Laminaria in Japan. Ise Bay. Suisanzoshoku 36(1): 1-6. Ii, A., K. Hasegawara & Katrashima, Experimental study on Laminaria cultivation in Hyogo prefecture. Suisanzoshoku 14(2): Kawashima, S., Kombu cultivation in Japan for human foodstuff. Jap. J. Phycol. 32: Kirihara, S., M. Notoya & Y. Aruga, Cultivation of Laminaria japonica at Hachinone, Aomori Prefecture, Japan. Korean J. Phycol. 4(2): Konbu Kyoukai, Production data of Laminaria. Konbu note. P.46, Nippon Kobu news paper Ltd. Matsuoka, M., M. Ohno & T. Akizuki, Growth of transplanted Laminaria japonica Areschoug in the culture ground of the Naruto straits in temperate waters. Suisanzoshoku 39(3): Ohno, M. & M. Matsuoka, Growth of cultivated Laminaria japonica, Undaria pinnatifida and U. undarioides in subtropical waters of Tosa. Suisanzoshoku 40(3): Sakai, H., Study on cultivated Laminaria japonica. Suisanzoshoku 1(4): Sanbonsuga, Y., Studies on the growth of forced Laminaria. Bull. Hokkaido Reg. Fish. Res. Lab. 49: Southgate, D.A.T., A procedure for the measurement of fats in foods. J. Sci. Food Agric. 22:90. Torkko, K., T. Ioriya, Y. Aruga & K. Iwamoto, Growth of transplanted Laminaria japonica Areschoug in Tokyo bay for from its natural habitat. Jap. J. Phycol. 3: Yotusi, T. & H. Nishikawa, Growing of cultivated transplanted Laminaria japonica Areschoug in Ariake Bay. Suisanzoshoku 1(4): References Achiha, H. & T. Nakamura, Growth and maturation of transplanted Laminaria japonica Areschoug in 10